Protein folds in channel structure

Current Opinion in Structural Biology

Volumn 6, Issue 4, 1996, Pages 499-510

  Montal, M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

CRYSTAL STRUCTURE; MEMBRANE CHANNEL; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW;

EID: 0030220255     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(96)80115-1     Document Type: Article

References (111)

1. Perutz M. Protein Structure. New Approaches To Disease And Therapy. 1992;WH Freeman, New York.
2. Orengo CA, Jones DJ, Thornton JM. Protein superfamilies and domain superfolds. Nature. 372:1994;631-634.
3. Govinddaraja S, Goldstein RA. Why are some protein structures so common? Proc Natl Acad Sci USA. 93:1996;3341-3345.
4. of special interest Panchenko AR, Luthey-Schulten Z, Wolynes PG. Foldons, protein structural modules, and exons. Proc Natl Acad Sci USA. 93:1996;2008-2013 An engaging analysis of the fundamental relationship between protein structural modules, exons and foldons - kinetically competent, quasi-independent folding units of a protein.
5. Leopold PE, Montal M, Onuchic JN. Protein folding funnels: a kinetic approach to the sequence - structure relationship. Proc Natl Acad Sci USA. 89:1992;8721-8725.
6. Montal M. Design of molecular function: channels of communication. Annu Rev Biophys Biomol Struct. 24:1995;31-57.
7. of special interest Montal M, Opella SJ. Assembly properties of model transmembrane channel peptides. von Heijne G. Membrane Protein Assembly. 1996;RG Landes, Texas, This paper describes an approach that determines channel protein structure by NMR. The secondary structure and details of the three-dimensional structure can be determined from multidimensional solution NMR experiments on peptides incorporated in detergent micelles. Solid-state NMR spectra of the peptides incorporated into oriented lipid bilayers provide direct information about the orientation of the peptide with respect to the membrane plane. The transmembrane structure of the channel-forming M2 segments of a choliner-gic, a glycinergic and a glutamatergic receptor channel has been determined by this approach.
8. Karlin A, Akabas M. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron. 15:1995;1231-1244.
9. Labarca C, Nowak MW, Zhang H, Tang L, Deshpande P, Lester HA. Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature. 376:1995;514-517.
10. Galzi JL, Changeux JP. Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr Opin Struct Biol. 4:1994;554-565.
11. of special interest Ferrer-Montiel AV, Montal M. Pentameric subunit stoichiometry of a neuronal glutamate receptor. Proc Natl Acad Sci USA. 93:1996;2741-2744 Two glutamate receptor subunits were specifically designed to exhibit differential sensitivity to open channel blockers. The expression of heteromeric receptors composed of varying ratios of sensitive to insensitive subunits, combined with blocker titration curves, allowed the determination of a pentameric subunit stoichiometry for GluR1.
12. Behe P, Stern P, Wyllie DJA, Nassar M, Schoepfer R, Colquhoun D. Determination of NMDAR NR1 subunit copy number in recombinant NMDA receptors. Proc R Soc Lond B Biol Sci. 262:1995;205-213.
13. Jonas P, Burnashev N. Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron. 15:1995;987-990.
14. of special interest Seeburg PH. The role of RNA editing in controlling glutamate receptor channel properties. J Neurochem. 66:1996;1-5 Offers a provocative insight into how RNA editing contributes to the functional diversity of glutamate receptors.
15. Ferrer-Montiel AV, Sun W, Montal M. A single tryptophan on M2 of glutamate receptor channels confers high permeability to divalent cations. Biophys J. 71:1996;. in press.
16. Catterall WA. Structure and function of voltage-gated ion channels. Annu Rev Biochem. 64:1995;493-531.
17. + channel T1 domain self-tetramerizes to a stable structure. J Biol Chem. 270:1995;28595-28600.
18. Xu J, Yu W, Jan YN, Jan LY, Li M. Assembly of voltage-gated potassium channels. Conserved hydrophilic motifs determine subfamily-specific interactions between the alpha-subunits. J Biol Chem. 270:1995;24761-24768.
19. Yu W, Xu J, Li M. NAB domain is essential for the subunit assembly of both α- and β- complexes of Shaker-like potassium channels. Neuron. 16:1996;441-453.
20. 2+ for gating and exhibiting a rectifying current - voltage relationship. Current efforts are directed towards introducing mutations into the P sequence aiming to alter selectivity, and to overproduce the protein for structural analysis (H Schrempf, personal communication).
21. Wickman K, Clapham DE. Ion channel regulation by G proteins. Physiol Rev. 75:1995;865-885.
22. Doupnik CA, Davidson N, Lester HA. The inward rectifier potassium channel family. Curr Opin Neurobiol. 5:1995;268-277.
23. + channel with a novel structure. EMBO J. 15:1996;1004-1011.
24. + channels nets yet more diversity. Neuron. 15:1995;489-492.
25. Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA. A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature. 376:1995;690-695.
26. + channel discovered by patch - clamp studies in 1986.
27. Deisenhofer J, Epp O, Sinning I, Michel H. Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol. 246:1995;429-457.
28. McDermott G, Prince SM, Freer AA, Hawthornthwaitelawless AM, Papiz MZ, Cogdell RJ, Isaacs NW. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature. 374:1995;517-521.
29. Koepke J, Hu X, Muenke C, Schulten K, Michel H. The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure. 4:1996;581-597.
30. of special interest Iwata S, Ostermeier C, Ludwig B, Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 376:1995;660-669 See annotation [31].
31. of special interest Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. The whole structure of the 13 subunit oxidized cytochrome oxidase at 2.8 Å Science. 272:1996;1136-1144 This study, together with [30], reveals the remarkable structure of bacterial [30] and mammalian [31] cytochrome oxidase. The multisubunit protein is predominantly α-helical. Pathways for the transfer of protons, electrons, oxygen and water are proposed. These structures are likely to provide a framework to delineate the pathways for proton pumping and its coupling to oxygen chemistry.
32. Subramaniam S, Gerstein MB, Oesterhelt D, Henderson R. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12:1993;1-8.
33. Havelka WA, Henderson R, Oesterhelt D. Three-dimensional structure of halorhodopsin at 7 Å resolution. J Mol Biol. 247:1995;726-738.
34. Schertler GF, Hargrave PA. Projection structure of frog rhodopsin in two crystal forms. Proc Natl Acad Sci USA. 92:1995;11578-11582.
35. Weiss MS, Schulz GE. Structure of porin refined at 1.8 Å resolution. J Mol Biol. 227:1992;493-509.
36. Schirmer T, Keller TA, Wang YF, Rosenbusch JP. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science. 267:1995;512-514.
37. Gouaux JE, Braha O, Hobaugh MR, Song L, Cheley S, Shustak C, Bayley H. Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc Natl Acad Sci USA. 91:1994;12828-12831.
38. Sheriff S, Hendrickson WA, Smith LJ. Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution. J Mol Biol. 197:1987;273-296.
39. Girvin ME, Fillingame RH. Determination of local protein structure by spin label difference 2D NMR: the region neighboring Asp61 of subunit c of the F1F0 ATP synthase. Biochemistry. 34:1995;1635-1645.
40. Sacchettini JC, Gordon JI, Banaszak LJ. Crystal structure of rat intestinal fatty-acid-binding protein. Refinement and analysis of the Escherichia coli-derived protein with bound palmitate. J Mol Biol. 208:1989;327-339.
41. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Karlavage AR, Dougherty BA, Merrick JM, et al. The minimal gene complement of Mycoplasma genitalium. Science. 270:1995;397-403.
42. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 269:1995;496-512.
43. Merritt EA, Sarfaty S, Chang TT, Palmer LM, Jobling MG, Holmes RK, Hol WG. Surprising leads for a cholera toxin receptor-binding antagonist: crystallographic studies of CTB mutants. Structure. 3:1995;561-570.
44. Cramer WA, Heymann JB, Schendel SL, Deriy BN, Cohen FS, Elkins PA, Stauffacher CV. Structure - function of the channel-forming colicins. Annu Rev Biophys Biomol Struct. 24:1995;611-641.
45. Bennett MJ, Choe S, Eisenberg D. Refined structure of dimeric diphtheria toxin at 2.0 Å resolution. Protein Sci. 3:1994;1444-1463.
46. L, an inhibitor of programmed cell death. Nature. 381:1996;335-341 The fold is similar to the membrane insertion domains of diphteria toxin [45] and colicin [44], and hints of a possible involvement of an ion-channel mechanism in apoptosis. In this respect, what the structure of diphteria toxin refined to 2 Å has revealed is significant [45]. The translocation domain consists of 10 helices of which four are transmembranous: residues in the transmembrane helices are buried in the structure but would be exposed by acid-induced unfolding, thereby promoting their insertion into the bilayer and consequent channel formation. Thus, helical bundles appear to be the structural blueprints for these channels.
47. of special interest Oblatt-Montal M, Yamazaki M, Nelson R, Montal M. Formation of ion channels in lipid bilayers by a peptide with the predicted transmembrane sequence of botulinum neurotoxin A. Protein Sci. 4:1995;1490-1497 Conformational energy calculations showed that a bundle of four amphipathic α helices is a plausible structural motif underlying the pore properties of the channel-forming peptide reconstituted in lipid bilayers.
48. Holm L, Sander C. Globin fold in a bacterial toxin. Nature. 361:1993;309.
49. Ladenstein R, Ritsert K, Huber R, Richter G, Bacher A. The lumazine synthase/riboflavin synthase complex of Bacillus subtilis. X-ray structure analysis of hollow reconstituted beta-subunit capsids. Eur J Biochem. 223:1994;1007-1017.
50. Unwin N. Nicotinic acetylcholine receptor at 9 Å resolution. J Mol Biol. 229:1993;1101-1124.
51. of special interest Unwin N. Acetylcholine receptor channel imaged in the open state. Nature. 373:1995;37-43 The major constriction in the image of the closed AChR appears at the location of L11 in the M2 sequence [51]. This arrangement may result from the constraints imposed on the five-helix bundle by its presence in the context of the entire protein. The major constriction in the pore pathway of the five-helix bundle of M2 helices is generated by a ring occurring at the location corresponding to F16 of the M2 sequence [52].
52. Montal MO, Iwamoto T, Tomich JM, Montal M. Design, synthesis and functional characterization of a pentameric channel protein that mimics the presumed pore structure of the nicotinic cholinergic receptor. FEBS Lett. 320:1993;261-266.
53. Breed J, Sankararamakrishnan R, Kerr ID, Sansom MSP. Molecular dynamics simulations of water within models of ion channels. Biophys J. 70:1996;1643-1661.
54. Oblatt-Montal M, Buhler LK, Iwamoto T, Tomich JM, Montal M. Synthetic peptides and four-helix bundle proteins as model systems for the pore-forming structure of channel proteins. I. Transmembrane segment M2 of the nicotinic cholinergic receptor channel is a key pore-limiting structure. J Biol Chem. 268:1993;14601-14607.
55. Bechinger B, Kim Y, Chirlian LE, Gesell J, Neumann JM, Tomich JM, Montal M, Zasloff M, Opella S. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J Biomol NMR. 1:1991;167-173.
56. Kato Y, Muto T, Tomura T, Tsumura H, Watarai H, Mikayama T, Ishizaka K, Kuroki R. The crystal structure of human glycosylation-inhibiting factor is a trimeric barrel with three 6-stranded β-sheets. Proc Natl Acad Sci USA. 93:1996;3007-3010.
57. Goldstein SAN. A structural vignette common to voltage sensors and conduction pores: canaliculi. Neuron. 16:1996;717-722.
58. Lu Q, Miller C. Silver as a probe of pore-forming residues in a potassium channel. Science. 268:1995;304-307.
59. Gross A, MacKinnon R. Agitoxin footprinting the Shaker potassium channel pore. Neuron. 16:1996;399-406.
60. + channel selectivity filter by mutant cycle-based structure analysis. Neuron. 16:1996;131-139 See annotation [61].
61. + channels. Taking advantage of the known three-dimensional structure of the scorpion toxins combined with scanning mutagenesis of the channel, pairs of interacting residues in the channel - toxin complex were identified.
62. + pore structure revealed by reporter cysteines at inner and outer surfaces. Neuron. 14:1995;1055-1063.
63. + channel probed by sulfhydryl-specific reagents after cysteine-scanning mutagenesis. Biophys J. 68:1995;900-905.
64. MacKinnon R. Pore loops: an emerging theme in ion channel structure. Neuron. 14:1995;889-892.
65. Perez-Garcia MT, Chiamvimonvat N, Marban E, Tomaselli GF. Structure of the sodium channel pore revealed by serial cysteine mutagenesis. Proc Natl Acad Sci USA. 93:1996;300-304.
66. Mande SC, Mehra V, Bloom BR, Hol WGJ. Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae. Science. 271:1996;203-207.
67. Hunt JF, Weaver AJ, Landry SJ, Gierasch L, Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature. 379:1996;37-45.
68. Heinemann SH, Terlau H, Stühmer W, Imoto K, Numa S. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature. 356:1992;441-443.
69. 2+ channel pore. FEBS Lett. 335:1993;265-269.
70. 2+ channels. Nature. 366:1993;158-161.
71. Zagotta WN, Siegelbaum SA. Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci. 19:1996;235-263.
72. 4: An ATP-activated ionotropic receptor cloned from rat brain. Proc Natl Acad Sci USA. 93:1996;3684-3688.
73. Kubo Y, Baldwin TJ, Jan YN, Jan LY. Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature. 362:1993;127-133.
74. Ho K, Nichols CG, Lederer WJ, Lytton J, Vassilev PM, Kanazirska MV, Hebert SC. Cloning and expression of an inwardly rectifying ATP-regulated potassium channel. Nature. 362:1993;31-38.
75. Yang N, George AL Jr, Horn R. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 16:1996;113-122.
76. Mannuzzu LM, Moronne MM, Isacoff EY. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 271:1996;213-216.
77. + channel S4. Neuron. 16:1996;387-397.
78. Mika YH, Palti Y. Charge displacements in a single potassium ion channel macromolecule during gating. Biophys J. 67:1994;1455-1463.
79. of special interest Doak DG, Mulvey D, Kawaguchi K, Villalain J, Campbell ID. Structural studies of synthetic peptides dissected from the voltage-gated sodium channel. J Mol Biol. 258:1996;672-687 The structure of synthetic peptides patterned after the sequence of predicted transmembrane segments of the voltage-gated sodium channel α subunit was determined by NMR and circular dirchromish spectroscopy. Peptides corresponding to S2, S3S4, S4 and the linker between S5 and S6, all from homologous repeat I, were found to have predominantly α-helical structures in trifluoroethanol and in dodecylphosphocholine micelles.
80. Greenblatt RE, Blatt Y, Montal M. The structure of the voltage-sensitive sodium channel: inferences derived from computer-aided analysis of the Electrophorus electricus channel primary structure. FEBS Lett. 193:1985;125-134.
81. + channels are due to the specific charge content of their respective S4 regions. Neuron. 10:1993;1121-1129.
82. + channels. Biophys J. 66:1994;345-354.
83. Stühmer W, Conti F, Suzuki H, Wang XD, Noda M, et al. Structural parts involved in activation and inactivation of the sodium channel. Nature. 339:1989;597-603.
84. Tytgat J, Nakazawa K, Gross A, Hess P. Pursuing the voltage sensor of a voltage-gated mammalian potassium channel. J Biol Chem. 268:1993;23777-23779.
85. + channel by three amino acid substitutions. Neuron. 16:1996;853-858.
86. + channel selectively modulates channel gating. Proc Natl Acad Sci USA. 92:1995;9422-9426 See annotation [87].
87. + channel play a role in modulating the voltage-dependent gating properties of the channel. These findings imply that S2 and S3, together with S4, may be components of the voltage-sensor module.
88. Luginbuhl P, Ottiger M, Mronga S, Wüthrich K. Structure comparison of the pheromones Er-1, Er-10, and Er-2 from Euplotes raikovi. Protein Sci. 3:1994;1537-1546.
89. Kuusinen A, Arvola M, Keinanen K. Molecular dissection of the agonist binding site of an AMPA receptor. EMBO J. 14:1995;6327-6332.
90. Stern-Bach Y, Bettler B, Hartley M, Sheppard PO, O'Hara PJ, Heinemann SF. Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron. 13:1994;1345-1357.
91. Hollmann M, Maron C, Heinemann S. N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron. 13:1994;1331-1343.
92. Sutcliffe MJ, Wo ZG, Oswald RE. Three-dimensional models of non-NMDA glutamate receptors. Biophys J. 70:1996;1575-1589.
93. Oh BH, Ames GF, Kim SH. Structural basis for multiple ligand specificity of the periplasmic lysine-, arginine-, ornithine-binding protein. J Biol Chem. 269:1994;26323-26330.
94. Kossiakoff AA, Somers W, Ultsch M, Andow K, Muller YA, De Vos AM. Comparison of the intermediate complexes of human growth hormone bound to the human growth hormone and prolactin receptors. Protein Sci. 3:1994;1697-1705.
95. Root MJ, MacKinnon R. Two identical noninteracting sites in an ion channel revealed by proton transfer. Science. 265:1994;1852-1856.
96. Sun ZP, Akabas MH, Goulding EH, Karlin A, Siegelbaum SA. Exposure of residues in the cyclic nucleotide-gated channel pore: P region structure and function in gating. Neuron. 16:1996;141-149.
97. Weber IT, Steitz TA. Structure of a complex of catabolite gene activator protein and cyclic AMP refined at 2.5 Å resolution. J Mol Biol. 198:1987;311-326.
98. Goulding EH, Tibbs GR, Siegelbaum SA. Molecular mechanism of cyclic-nucleotide-gated channel activation. Nature. 372:1994;369-374.
99. Varnum MD, Black KD, Zagotta WN. Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels. Neuron. 15:1995;619-625.
100. Gordon SE, Zagotta WN. Localization of regions affecting an allosteric transition in cyclic nucleotide-activated channels. Neuron. 14:1995;857-864.
101. of special interest Trudeau MC, Warmke JW, Ganetzky B, Robertson GA. HERG, a human inward rectifier in the voltage-gated potassium channel family. Science. 269:1995;92-95 See annotation [102].
102. of special interest Sanguinetti MC, Jiang C, Curran M, Keating MT. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell. 81:1995;299-307 These two papers [101,102] show that the Kv channel superfamily also includes channels that exhibit voltage-dependent gating modulated by cyclic AMP, suggesting a fusion of a Kv with a cyclic AMP-binding modulatory module.
103. Slesinger PA, Reuveny E, Jan YN, Jan LY. Identification of structural elements involved in G protein gating of the GIRK1 potassium channel. Neuron. 15:1995;1145-1156.
104. + channel proteins. Nature. 374:1995;135-141.
105. + channels are activated by G βγ-subunits and function as heteromultimers. Proc Natl Acad Sci USA. 92:1995;6542-6546.
106. + channel by G-protein α-subunits. Nature. 380:1996;624-627.
107. Minor DL Jr, Kim PS. Context-dependent secondary structure formation of a designed protein sequence. Nature. 380:1996;730-734.
108. Do H, Falcone D, Liu J, Andrews DW, Johnson AE. The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell. 85:1996;369-378.
109. + channel surface expression through effects early in biosynthesis. Neuron. 16:1996;843-852.
110. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr. 24:1991;946-950.
111. Smart OS, Goodfellow JM, Wallace BA. The pore dimensions of gramicidin A. Biophys J. 65:1993;2455-2460.